Effects of period RNAi on V-ATPase expression and rhythmic pH changes in the vas deferens of Spodoptera littoralis (Lepidoptera: Noctuidae)

Insect Biochemistry and Molecular Biology

Volumn 43, Issue 6, 2013, Pages 522-532

  Kotwica Rolinska, Joanna ^a   Gvakharia, Barbara O ^b   Kedzierska, Urszula ^a   Giebultowicz, Jadwiga M ^b   Bebas, Piotr ^a  

^a UNIVERSITY OF WARSAW   (Poland)

^b OREGON STATE UNIVERSITY   (United States)

Author keywords

Biological clock; Period; Peripheral oscillators; RNAi; Spodoptera littoralis; V ATPase

Indexed keywords

PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; TRANSCRIPTION FACTOR CLOCK;

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; CIRCADIAN RHYTHM; ENZYMOLOGY; EPITHELIUM; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MALE; METABOLISM; PH; PHYSIOLOGY; REPRODUCTION; RNA INTERFERENCE; SPERMATOZOON; SPODOPTERA; TESTIS;

ANIMALS; BEHAVIOR, ANIMAL; CIRCADIAN CLOCKS; CLOCK PROTEINS; EPITHELIUM; GENE EXPRESSION REGULATION; HYDROGEN-ION CONCENTRATION; MALE; REPRODUCTION; RNA INTERFERENCE; SPERMATOZOA; SPODOPTERA; TESTIS; VACUOLAR PROTON-TRANSLOCATING ATPASES;

ALABAMA ARGILLACEA; GOSSYPIUM HIRSUTUM; HEXAPODA; LEPIDOPTERA; NOCTUIDAE; SPODOPTERA LITTORALIS;

EID: 84877027521     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2013.03.002     Document Type: Article

References (66)

1. Abruzzi K.C., Rodriguez J., Menet J.S., Desrochers J., Zadina A., Luo W., Tkachev S., Rosbash M. Drosophila CLOCK target gene characterization: implications for circadian tissue-specific gene expression. Genes Dev. 2011, 25:2374-2386.
2. Allada R., Chung B.Y. Circadian organization of behavior and physiology in Drosophila. Annu. Rev. Physiol. 2010, 72:605-624.
3. Bebas P., Cymborowski B. Effects of constant light on male sterility in Spodoptera litttoralis (Lepidoptera: Noctuidae). Physiol. Entomol. 1999, 24:165-170.
4. Bebas P., Cymborowski B., Giebultowicz J.M. Circadian rhythm of sperm release in males of the cotton leafworm, Spodoptera littoralis: in vivo and in vitro study. J. Insect Physiol. 2001, 47:859-866.
5. +-ATPase. J. Exp. Biol. 2002, 205:37-44.
6. Bebas P., Goodall C.P., Majewska M., Neumann A., Giebultowicz J.M., Chappell P.E. Circadian clock and output genes are rhythmically expressed in extratesticular ducts and accessory organs of mice. FASEB J. 2009, 23:523-533.
7. Bebas P., Maksimiuk E., Gvakharia B.O., Cymborowski B., Giebultowicz J.M. Circadian rhythm of glycoprotein secretion in the vas deferens of moth, Spodoptera littoralis. BMC Physiol. 2002, 2:15.
8. Bloch G., Hazan E., Rafaeli A. Circadian rhythms and endocrine functions in adult insects. J. Insect Physiol. 2012, http://dx.doi.org/10.1016/j.jinsphys.2012.10.012.
9. Brouns I., Van Nassauw L., Van Genechten J., Majewski M., Scheuermann D.W., Timmermans J.P., Adriaensen D. Triple immunofluorescence staining with antibodies raised in the same species to study the complex innervation pattern of intrapulmonary chemoreceptors. J. Histochem. Cytochem. 2002, 50:575-582.
10. Brown D., Breton S. H(+)V-ATPase-dependent luminal acidification in the kidney collecting duct and the epididymis/vas deferens: vesicle recycling and transcytotic pathways. J. Exp. Biol. 2000, 203:137-145.
11. Ceriani M.F., Hogenesch J.B., Yanovsky M., Panda S., Straume M., Kay S.A. Genome-wide expression analysis in Drosophila reveals genes controlling circadian behavior. J. Neurosci. 2002, 22:9305-9319.
12. Edery I., Zwiebel L.J., Dembinska M.E., Rosbash M. Temporal phosphorylation of the Drosophila period protein. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:2260-2264.
13. Filippova M., Ross L.S., Gill S.S. Cloning of the V-ATPase B subunit cDNA from Culex quinquefasciatus and expression of the B and C subunits in mosquitoes. Insect Mol. Biol. 1998, 7:223-232.
14. Giebultowicz J.M., Bell R.A., Imberski R.B. Circadian rhythm of sperm movement in the male reproductive tract of the gypsy moth, Lymantria dispar. J. Insect Physiol. 1988, 34:527-532.
15. Giebultowicz J.M., Blackburn M.B., Thomas-Laemont P.A., Raina A.K. Sterilization of the gypsy moth by disruption of sperm release from testis. Pest Management: Biologically Based Technologies 1993, 114-116. American Chemical Society, Washington, D.C. R.D. Lumsden, J.L. Vaughn (Eds.).
16. Giebultowicz J.M., Brooks N.L. The circadian rhythm of sperm release in the codling moth, Cydia pomonella. Ent. Exp. Appl. 1998, 88:229-234.
17. Giebultowicz J.M., Joy J.E., Riemann J.G., Raina A.K. Changes in protein pattern in sperm and vas deferens during the daily rhythm of sperm release in the gypsy moth. Arch. Insect Biochem. Physiol. 1994, 25:317-327.
18. Giebultowicz J.M., Ridgway R.L., Imberski R.B. Physiological basis for sterilizing effects of constant light in Lymantria dispar. Physiol. Entomol. 1990, 15:149-156.
19. Giebultowicz J.M., Riemann J.G., Raina A.K., Ridgway R.L. Circadian system controlling release of sperm in the insect testes. Science 1989, 245:1098-1100.
20. Gvakharia B.O., Bebas P., Cymborowski B., Giebultowicz J.M. Disruption of sperm release from insect testes by cytochalasin and beta-actin mRNA mediated interference. Cell. Mol. Life Sci. 2003, 60:1744-1751.
21. Gvakharia B.O., Kilgore J.A., Bebas P., Giebultowicz J.M. Temporal and spatial expression of the period gene in the reproductive system of the codling moth. J. Biol. Rhythms 2000, 15:27-35.
22. Hardin P.E. Molecular genetic analysis of circadian timekeeping in Drosophila. Adv. Genet. 2011, 74:141-173.
23. Hassaneen E., El-Din Sallam A., Abo-Ghalia A., Moriyama Y., Karpova S.G., Abdelsalam S., Matsushima A., Shimohigashi Y., Tomioka K. Pigment-dispersing factor affects nocturnal activity rhythms, photic entrainment, and the free-running period of the circadian clock in the cricket Gryllus bimaculatus. J. Biol. Rhythms 2011, 26:3-13.
24. Ikeno T., Numata H., Goto S.G. Circadian clock genes period and cycle regulate photoperiodic diapause in the bean bug Riptortus pedestris males. J. Insect Physiol. 2011, 57:935-938.
25. Ikeno T., Numata H., Goto S.G. Photoperiodic response requires mammalian-type cryptochrome in the bean bug Riptortus pedestris. Biochem. Biophys. Res. Commun. 2011, 410:394-397.
26. Iwai S., Fukui Y., Fujiwara Y., Takeda M. Structure and expressions of two circadian clock genes, period and timeless in the commercial silkmoth, Bombyx mori. J. Insect Physiol. 2006, 52:625-637.
27. Kamae Y., Tomioka K. Timeless is an essential component of the circadian clock in a primitive insect, the firebrat Thermobia domestica. J. Biol. Rhythms 2012, 27:126-134.
28. Kotwica J., Bebas P., Gvakharia B.O., Giebultowicz J.M. RNA interference of the period gene affects the rhythm of sperm release in moths. J. Biol. Rhythms 2009, 24:25-34.
29. Kotwica J., Ciuk M.A., Joachimiak E., Rowinski S., Cymborowski B., Bebas P. Carbonic anhydrase activity in the vas deferens of the cotton leafworm - Spodoptera littoralis (Lepidoptera: Noctuidae) controlled by circadian clock. J. Physiol. Pharmacol. 2006, 57(Suppl. 8):107-123.
30. Kotwica J., Joachimiak E., Polanska M.A., Majewska M.M., Giebultowicz J.M., Bebas P. Diurnal rhythm in expression and release of yolk protein in the testis of Spodoptera littoralis (Lepidoptera: Noctuidae). Insect Biochem. Mol. Biol. 2011, 41:264-272.
31. Kotwica J., Larson M.K., Bebas P., Giebultowicz J.M. Developmental profiles of PERIOD and DOUBLETIME in Drosophila melanogaster ovary. J. Insect Physiol. 2009, 55:419-425.
32. Lee C.M., Su M.T., Lee H.J. Pigment dispersing factor: an output regulator of the circadian clock in the German cockroach. J. Biol. Rhythms 2009, 24:35-43.
33. Moriyama Y., Sakamoto T., Karpova S.G., Matsumoto A., Noji S., Tomioka K. RNA interference of the clock gene period disrupts circadian rhythms in the cricket Gryllus bimaculatus. J. Biol. Rhythms 2008, 23:308-318.
34. Negoescu A., Labat-Moleur F., Lorimier P., Lamarcq L., Guillermet C., Chambaz E., Brambilla E. F(ab) secondary antibodies: a general method for double immunolabeling with primary antisera from the same species. Efficiency control by chemiluminescence. J. Histochem. Cytochem. 1994, 42:433-437.
35. Pietrantonio P.V., Gill S.S. Immunolocalization of the 17 kDa vacuolar H(+)-ATPase subunit c in Heliothis virescens midgut and malpighian tubules with an anti-peptide antibody. J. Exp. Biol. 1995, 198:2609-2618.
36. Pyza E., Borycz J., Giebultowicz J.M., Meinertzahagen I.A. Involvement of V-ATPase in the regulation of cell size in the fly's visual system. J. Insect Physiol. 2004, 50:985-994.
37. Riemann J.G., Giebultowicz J.M. Secretion in the upper vas deferens of the gypsy moth correlated with the circadian rhythm of sperm release from the testes. J. Insect Physiol. 1991, 37:53-62.
38. Riemann J.G., Ruud R.L. Mediterranean flour moth: effects of continuous light on the reproductive capacity. Ann. Entomol. Soc. Am. 1974, 67:857-860.
39. Riemann J.G., Thorson B.J. Ultrastructure of the vasa deferentia of the Mediterranean flour moth. J. Morphol. 1976, 149:483-506.
40. Riemann J.G., Thorson B.J., Ruud R.L. Daily cycle of release of sperm from the testes Mediterranean flour moth. J. Insect Physiol. 1974, 20:195-207.
41. Rund S.S., Hou T.Y., Ward S.M., Collins F.H., Duffield G.E. Genome-wide profiling of diel and circadian gene expression in the malaria vector Anopheles gambiae. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:E421-E430.
42. Sandrelli F., Cappellozza S., Benna C., Saviane A., Mastella A., Mazzotta G.M., Moreau S., Pegoraro M., Piccin A., Zordan M.A., Cappellozza L., Kyriacou C.P., Costa R. Phenotypic effects induced by knock-down of the period clock gene in Bombyx mori. Genet. Res. 2007, 89:73-84.
43. Sandrelli F., Costa R., Kyriacou C.P., Rosato E. Comparative analysis of circadian clock genes in insects. Insect Mol. Biol. 2008, 17:447-463.
44. Sauman I., Reppert S.M. Circadian clock neurons in the silkworm, Antheraea pernyi: Novel mechanism of period protein regulation. Neuron 1996, 17:889-900.
45. Sauman I., Reppert S.M. Brain control of embryonic circadian rhythms in the silkworm, Antheraea pernyi. Neuron 1998, 20:741-748.
46. Schuckel J., Siwicki K.K., Stengl M. Putative circadian pacemaker cells in the antenna of the hawkmoth Manduca sexta. Cell. Tissue Res. 2007, 330:271-278.
47. Sehadova H., Markova E.P., Sehnal F., Takeda M. Distribution of circadian clock-related proteins in the cephalic nervous system of the silkworm, Bombyx mori. J. Biol. Rhythms 2004, 19:466-482.
48. Shao Q.M., Sehadova H., Ichihara N., Sehnal F., Takeda M. Immunoreactivities to three circadian clock proteins in two ground crickets suggest interspecific diversity of the circadian clock structure. J. Biol. Rhythms 2006, 21:118-131.
49. Sun-Wada G.H., Wada Y., Futai M. Diverse and essential roles of mammalian vacuolar-type proton pump ATPase: toward the physiological understanding of inside acidic compartments. Biochim. Biophys. Acta 2004, 1658:106-114.
50. Takekata H., Matsuura Y., Goto S.G., Satoh A., Numata H. RNAi of the circadian clock gene period disrupts the circadian rhythm but not the circatidal rhythm in the mangrove cricket. Biol. Lett. 2012, 8:488-491.
51. Terenius O., Papanicolaou A., Garbutt J.S., Eleftherianos I., Huvenne H., Kanginakudru S., Albrechtsen M., An C., Aymeric J.L., Barthel A., Bebas P., Bitra K., Bravo A., Chevalier F., Collinge D.P., Crava C.M., de Maagd R.A., Duvic B., Erlandson M., Faye I., Felfoldi G., Fujiwara H., Futahashi R., Gandhe A.S., Gatehouse H.S., Gatehouse L.N., Giebultowicz J.M., Gomez I., Grimmelikhuijzen C.J., Groot A.T., Hauser F., Heckel D.G., Hegedus D.D., Hrycaj S., Huang L., Hull J.J., Iatrou K., Iga M., Kanost M.R., Kotwica J., Li C., Li J., Liu J., Lundmark M., Matsumoto S., Meyering-Vos M., Millichap P.J., Monteiro A., Mrinal N., Niimi T., Nowara D., Ohnishi A., Oostra V., Ozaki K., Papakonstantinou M., Popadic A., Rajam M.V., Saenko S., Simpson R.M., Soberon M., Strand M.R., Tomita S., Toprak U., Wang P., Wee C.W., Whyard S., Zhang W., Nagaraju J., Ffrench-Constant R.H., Herrero S., Gordon K., Swevers L., Smagghe G. RNA interference in Lepidoptera: an overview of successful and unsuccessful studies and implications for experimental design. J. Insect Physiol. 2011, 57:231-245.
52. Tobback J., Boerjan B., Vandersmissen H.P., Huybrechts R. The circadian clock genes affect reproductive capacity in the desert locust Schistocerca gregaria. Insect Biochem. Mol. Biol. 2011, 41:313-321.
53. Tobback J., Boerjan B., Vandersmissen H.P., Huybrechts R. Male reproduction is affected by RNA interference of period and timeless in the desert locust Schistocerca gregaria. Insect Biochem. Mol. Biol. 2012, 42:109-115.
54. Tomioka K., Matsumoto A. A comparative view of insect circadian clock systems. Cell. Mol. Life Sci. 2009, 67:1397-1406.
55. Tomioka K., Uryu O., Kamae Y., Umezaki Y., Yoshii T. Peripheral circadian rhythms and their regulatory mechanism in insects and some other arthropods: a review. J. Comp. Physiol. B 2012, 182:729-740.
56. Wada Y., Sun-Wada G.H., Tabata H., Kawamura N. Vacuolar-type proton ATPase as regulator of membrane dynamics in multicellular organisms. J. Bioenerg. Biomembr. 2008, 40:53-57.
57. Weevers R.G.J. A lepidopteran saline: effects of inorganic cation concentrations on sensory, reflex and motor responses in a herbivorous insect. J. Exp. Biol. 1966, 44:163-175.
58. Wen C.J., Lee H.J. Mapping the cellular network of the circadian clock in two cockroach species. Arch. Insect Biochem. Physiol. 2008, 68:215-231.
59. Wieczorek H., Beyenbach K.W., Huss M., Vitavska O. Vacuolar-type proton pumps in insect epithelia. J. Exp. Biol. 2009, 212:1611-1619.
60. Wieczorek H., Brown D., Grinstein S., Ehrenfeld J., Harvey W.R. Animal plasma membrane energization by proton-motive V-ATPases. Bioessays 1999, 21:637-648.
61. Wieczorek H., Grüber G., Harvey W.R., Huss M., Merzendorfer H., Zeiske W. Structure and regulation of insect plasma membrane H(+)V-ATPase. J. Exp. Biol. 2000, 203:127-135.
62. Wijnen H., Naef F., Boothroyd C., Claridge-Chang A., Young M.W. Control of daily transcript oscillations in Drosophila by light and the circadian clock. PLoS Genet. 2006, 2:e39.
63. Wise S., Davis N.T., Tyndale E., Noveral J., Folwell M.G., Bedian V., Emery I.F., Siwicki K.K. Neuroanatomical studies of period gene expression in the hawkmoth, Manduca sexta. J. Comp. Neurol. 2002, 447:366-380.
64. Yamazaki S., Numano R., Abe M., Hida A., Takahashi R., Ueda M., Block G.D., Sakaki Y., Menaker M., Tei H. Resetting central and peripheral circadian oscillators in transgenic rats. Science 2000, 288:682-685.
65. Yang Y.Y., Wen C.J., Mishra A., Tsai C.W., Lee H.J. Development of the circadian clock in the German cockroach, Blattella germanica. J. Insect Physiol. 2009, 55:469-478.
66. Zavodska R., Sauman I., Sehnal F. Distribution of PER protein, pigment-dispersing hormone, prothoracicotropic hormone, and eclosion hormone in the cephalic nervous system of insects. J. Biol. Rhythms 2003, 18:106-122.